Tag Archives: herbivory

Those of you whom work in forests, will, I am sure, be familiar with the term “green island”. To a forester or forest entomologist, a green island is a clump of trees that have, for some reason or other, survived the ravages of an insect outbreak. The earliest reference I can find to this phenomenon is in a 1927 paper by the German myrmecologist Hermann Eidmann (1897-1949), who described them as green oases, or, as the paper was written in German, more correctly, “grüne Oasen” (Eidmann, 1927).

As well as “farming aphids” to obtain sugar from their honeydew, ants also have a similar mutualistic relationship with plants that give them a sugary reward to protect them from herbivorous insects, except those that also provide the ants with sugar (Janzen 1966; Bentley, 1977). The mutualisms can be very sophisticated. In Michigan, the North American black cherry, Prunus serotina, times nectar production from its extra-floral nectaries to attract the ant Formica obscuripes when the larvae of its major herbivore, the eastern tent caterpillar, Malacosoma americanum are at their most vulnerable (Tilman, 1978). Trees that are protected have greatly reduced levels of herbivory. When more than one ant colony is involved, rather than single trees being protected, a group of trees can be saved from defoliation, and form a green island. The areas covered by these green islands can be quite extensive, for example two ant colonies of the ant Formica polyctena were enough to protect pine trees from the nun moth Lymantria monacha in Sweden within a 45 m diameter around the colonies (0.16 ha) (Wellenstein, 1980) and green islands of up to 3 ha have been reported (Eidmann, 1927).

Left – canopy of trees near ant nests, on the right, trees not close to ant nests Wellenstein (1980)

In Finland, one colony of the ant F. aquilonia is enough to create subarctic mountain birch (Betula pubescens), green islands of up to 0.12 ha in area (Laine & Niemelä, 1980).

It would seem that the case for the ants protecting the trees against defoliating herbivores and being the cause for the green islands is very convincing. Tom White, never one to avoid a controversy, disagreed. He suggested that it was the nest building activities of the ants that were the cause for the green islands, the refuse dumps provide higher concentrations of nutrients that the roots of surrounding trees can access and additionally soil moisture conditions are improved, both these factors encouraging more vigorous growth in those trees close to ant nests, making them less palatable to herbivores (White, 1985). The Finnish team responded to this with some additional data and arguments defending their hypothesis (Niemelä & Laine, 1986) and there the matter rested, for a while at least. Not satisfied with their post hoc response, the Finns came up with, to me at any rate, a very convincing field experiment where they showed that soil nitrogen did not vary significantly with distance from ant nests and that birch leaf nitrogen content and moth larval growth rates and survival were also not affected by distance from ant nests (Karhu, 1998; Karhu & Neuvonen, 1998), indicating that the green islands were indeed, due to predation by the ants and not improved tree nutrition.

You might think that this would be the last word, but you would be wrong 🙂 The Karhu and Neuvonen paper, is, in the journal, followed by a “comment” paper by no less a person than Tom White (White 1998) in which he disputes in no uncertain terms, their interpretation of their new data. Matthias Schaefer, the then Editor of Oecologia, felt that some sort of explanation was needed and added a final note to the saga, which in itself makes very interesting reading. I get the feeling that there were some strong emotions involved 🙂

In 1981 I spent a lot of time trudging through snow, cross-country skiing and snow-shoeing my way across the snowy wastes of Finland to snip twigs off bird cherry trees. This was part of my post-doc which was to develop a forecasting system for the bird cherry-oat aphid, Rhopalosiphum padi. On returning to the lab I then spent many a happy hour counting how many aphid eggs were nestled in between the buds and the stem on each twig. It was while doing this that I noticed that some of the twigs were infested with the overwintering larval shields of the bird cherry ermine moth, Yponomeuta evonymellus. Of course I then started counting them as well 🙂 I noticed that trees with lots of aphid eggs didn’t have very many larval shields and I wondered why. Some later observations from marked trees in Scotland appeared to provide evidence that the aphids and the moths tended to either prefer different trees or perhaps excluded each other.

Based on these data I hypothesised that the two insects were indirectly competing for resources by altering plant chemistry and/or architecture thus making the trees less or more suitable for egg laying in the autumn (Leather, 1988). I tested this experimentally when I was working for the Forestry Commission in Scotland using potted bird cherry trees that I defoliated to a lesser or greater extent to see if I could induce changes in foliar quality and tree growth rates that might influence subsequent colonisation by the aphids and moths. As predicted, those trees that had been defoliated, albeit by me and not by moth larvae, were less attractive to aphids in the autumn (Leather, 1993). These effects were still apparent five years after the beginning of the experiment (Leather, 1995) when I had to desert my trees as I moved to a new position at Imperial College’s Silwood Park campus.

Given that apart from the location, the SE of England, this was my idea of a dream job for life (colleagues at the time included John Lawton, Mike Hassell, Bob May, Stuart McNeill, Mike Way, Brad Hawkins, Shahid Naeem, Mike Hochberg, Chris Thomas to name but a few), I decided to start up two long-term projects to see me through the next 30 years, one observational (my 52 sycamore tree project), the other experimental, a follow up to my bird cherry defoliation experiment.

I went for a simplified design of my earlier experiments, just two defoliation regimes, one to mimic aphid infestation (50%), the other to mimic bird cherry ermine moth defoliation (100%) and of course a non-defoliated control. I also planted the trees in the ground to better simulate reality. Using potted plants is always a little suspect and I figured that I would need to do rather a lot of re-potting over the next 30 years 🙂

The grand plan!

I sourced my trees from a Forestry Commission nursery thinking that as the national organisation responsible for tree planting in the UK I could trust the provenance of the trees. Things didn’t go well from the start. Having planted my trees in autumn 1992 and established the treatments in the spring of 1993 I discovered that my bird cherry, rather than being from a native provenance (seed origin) were originally from Serbia! Hmm 🙂 It was too late to start again, so I decided to carry on. After all, bird cherry although widely planted in the SE, has a native distribution somewhat further north and west, which meant I was already operating close to the edge of ‘real life’, so what did an extra 1600 kilometres matter?

Next, I discovered that my fence was neither rabbit nor deer proof. I almost gave up at this point, but having invested a lot of time and energy in setting up the plot I once again decided to carry on. On the plus side, the trees most heavily defoliated and bitten back were mainly from the 100% defoliation treatment, but did give me some negative growth rates in that year.

My original plan was to record height (annually), bird cherry egg numbers (every December), bird cherry ermine moth larval shields (annually), bud burst and leaf expansion once a week, leaf-fall (annually), and once a month, defoliation rates in two ways, number of damaged leaves and an overall estimation of percentage defoliation. This was a personal project, so no grant funding and no funding for field assistants. It soon became clear, especially when my teaching load grew, as Imperial started replacing whole organism biologists with theoretical and molecular biologists, and I was drafted in to take on more and more of the whole organism lecturing, that I would not be able to keep both of my long term projects going with the same intensity. Given the ‘problems’, associated with the bird cherry project, I decided that I would ditch some of my sampling, bud burst was scored on 21st March every year and defoliation only measured once, in late summer and egg sampling and height recording came to a halt once the trees grew above me (2005)! This allowed me to carry on the sycamore project as originally intended*.

I kept an eye on the trees until I left Silwood Park in 2012, but by 2006 I was only monitoring bud burst and leaf fall feeling that this might be useful for showing changes in phenology in our ever-warming world. One regret as I wandered between the then sizeable trees in the autumn of 2012 was that I had not taken a before and after photograph of the plots. All I have are two poor quality photos, one from 2006, the other from 2012.

The Sixty Tree site April 2006.

The Sixty Tree site April 2010 with a very obvious browse line

So, after all the investment in time, and I guess to a certain extent money (the trees and the failed fencing, which both came out of my meagre start-up funding**), did anything worthwhile come out of the study?

The mean number of Rhopalosiphum padi eggs per 100 buds in relation to defoliation treatment

As a long-time fan of aphid overwintering it was pleasing to see that there was a significant difference not only between years (F= 8.9, d.f. = 9/29, P <0.001), but also between treatments with the trees in the control treatment having significantly more eggs laid on them than the 100% defoliation treatment (F= 9.9, d.f. = 2/ 29, P <0.001 with overall means of 1.62, 1.22 and 0.65 eggs/100 buds). This also fitted in with the hypothesis that trees that are defoliated by chewing herbivores become less suitable for aphids (Leather, 1988). I must admit that this was a huge surprise to me as I had thought that as all the trees were attacked by deer the year after the experimental treatments they would all respond similarly, which is why I almost gave up the experiment back in 1994.

Bud burst stage of Prunus padus at Silwood Park on March 21st 1996-2012; by treatment and combined

When it came to budburst there was no treatment effect, but there was a significant trend to earlier budburst as the trees became older which was strongly correlated with warmer springs, although as far as spring temperatures were concerned there was no significant increase with year.

Mean date of final leaf fall of Prunus padus at Silwood Park 1995-2012; by treatment and combined

At the other end of the year, there was a significant difference between date of final leaf fall between years but no significant difference between treatments. In retrospect I should have adopted another criterion. My date for final leaf fall was when the last leaf fell from the tree. Those of you who have watched leaves falling from trees will know that there are always a few who are reluctant to make that drop to the ground to become part of the recycling process. Even though they are very obviously dead, they hang there until finally dislodged by the wind. I should really have used a measure such as last leaf with any pigment remaining. I am sure that if I could be bothered to hunt down the wind speed data I would find that some sort of correlation.

Mean height (cm) of Prunus padus trees at Silwood Park 1993-2005 and Diameter at Breast Height (DBH) (cm) at the end of 2012

Except for the year after the deer attack, the trees, as expected, grew taller year by year. There was however, no significant difference between heights reached by 2005 or in DBH at the end of 2012 despite what looked like a widening gap between treatments.

My original hypothesis that trees that were heavily defoliated at the start of their life would be more susceptible to chewing insects in later life, was not supported. There was no significant difference between treatments, although, not surprisingly, there was a significant difference between years. Average defoliation as has been reported for other locations was about 10% (Kozlov et al., 2015; Lim et al., 2015).

Number of Prunus padus trees with severe deer damage

That said, when I looked at the severity of deer attack, there was no effect of year but there was a significant effect of treatment, those trees that had been 100% defoliated in 1993 being most attractive to deer. In addition, 20% of those trees were dead by 2012 whereas no tree deaths occurred for the control and less severely defoliated treatments.

I confess to being somewhat surprised to find as many significant results as I did from this simple analysis and was momentarily tempted to do a more formal analysis and submit it to a journal. Given, however, the number of confounding factors, I am pretty certain that I would be looking at an amateur natural history journal with very limited visibility. Publishing it on my blog will almost certainly get it seen by many more people, and who knows may inspire someone to do something similar but better.

The other reason that I can’t be bothered to do a more formal analysis is that my earlier work on which this experiment was based has not really hit the big time, the four papers in question only accruing 30 cites between them. Hardly earth shattering despite me thinking that it was a pretty cool idea; insects from different feeding guilds competing by changing the architecture and or chemsitry of their host plant. Oh well. Did anything come out of my confounded experiment or was it a total waste of time? The only thing published from the Sixty Trees was a result of a totally fortuitous encounter with Marco Archetti and his fascination with autumn colours (Archetti & Leather, 2005), the story of which I have related in a previous post, and which has, in marked contrast to the other papers, had much greater success in the citation stakes 🙂

And finally, if anyone does want to play with the data, I am very happy to give you access to the files.

Leather, S.R. (1985) Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology, 10, 43-56. 14 cites

Journal clubs have been around a long time, but as a new PhD student in 1977 it was a new experience for me. I was thus somewhat uncertain about what was expected from me when my supervisor presented me with a copy of Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492, and informed me that I was going to present my views on the paper the following month. In those days organised PhD training programmes in the UK did not exist. Nowadays, PhD students in the UK follow a programme of lectures and workshops ranging from statistics, presentation skills, paper writing, ethics, use of social media, how to run tutorials, IPR, critical appraisal, etc. etc. Given my lack of experience, I was a little apprehensive to say the least. Luckily I had the chance to see how the older members of our research group dealt with their papers in the preceding weeks and was somewhat moe confident about what was expected of me. I duly read the paper and highlighted the areas that I wanted to critique.

Parts of the Owen & Weigert (1976) paper showing the bits that I highlighted for my critique.

Owen & Weigert’s hypothesis was, that contrary to accepted doctrine, consumers, especially those feeding on trees, were beneficial to their host plants and not harmful. Coming fresh from an agriculture department where I had been taught that anything that ate a plant was a pest, this was a startling and heretical concept for me to digest! I remember at the time that I was not particularly convinced by the arguments and that within the group the general consensus was that Denis Owen was a bit of an eccentric. In fact, the senior members of the group entered into a printed debate in the popular scientific press (McLean et al., 1977; Owen, 1977) which resulted in what I still consider to be the best ever front cover of New Scientist 😉

Arguably the best ever front cover of New Scientist

We were not the only ones who expressed scepticism about Owen’s hypothesis, although experimental rebuttals of Owen’s claim that aphids and trees were in a mutualistic relationship via honeydew production did not appear until some years later (Petelle, 1980; Choudhury, 1984, 1985). These papers resulted in a series of spirited responses from Owen (Owen & Wiegert, 1982a, b, 1985, 1987). Some years later, however, Joy Belsky provided further evidence against Owen’s hypothesis (Belsky, 1986,1987; Belsky et al., 1993) and I too entered the fray (Leather, 1988,2000).

Thus by the end of the last century it appeared that all the evidence indicated that if you were a plant, being eaten was not good for you. On the other hand, if Owen had posed his hypothesis at a population or group level, he might have been able to make a better case for herbivores increasing plant fitness. In an earlier post, in which I wrote about the plant immune response and how plants communicate with each other when attacked and warn their neighbours of potential attack, one could definitely make a stronger case for plants benefitting from being eaten. Induced resistance can even work at an individual level, some recent work (McArt et al., 2013) has shown that evening primroses (Oenothera biennis) attacked early in the season by the Japanese beetle, Popillia japnonica, become more resistant to attack from seed predators than those that escape early season defoliation. As a result the beetle attacked plants produce more seed than those that escaped attack. Given that a general measure of fitness is reproductive success (i.e. how many seeds are produced) then in this case, consumers do maximise plant fitness and Denis Owen can have the last word.

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